After all: Xenoturbella is an acoelomorph!

Abstract

Xenoturbella (Fig. 1) is a centimeter-long, flattened, oval,completely ciliated ‘‘worm’’ with a mid-ventral gut opening; itis rather common on various substrates at 40–100m depthsalong the Swedish west coast. It was originally studied bySixten Bock and subsequently described by Westblad (1950)with incorporation of Bock’s material. Westblad interpretedXenoturbella as a primitive turbellarian, based on the generalmorphology, including the structure of epithelia, nervoussystem, statocyst, musculature, endoderm, and gonads. Hepointed out that the animal resembles unspecialized turbell-arians in almost all characters, except the gonads. The gonadsconsist of scattered oocytes/eggs and spermatocytes/sperm inthe parenchyme; there is no copulatory organ equivalent tothat characteristic of other flatworms, and the gametes appearto be spawned through the gut and the mouth opening. Hepointed to similarities with other primitive turbellarians, suchas acoels and nemertodermatids, especially in the nervoussystem; but also to differences, such as the thick parenchyme,which is not found in the acoelomorphs. He erected the newsuborder Xenoturbellida, placed at the base of the arcoopho-ran Platyhelminthes. The description inspired a number ofquite imaginative speculations (review in Reisinger 1960), butmost textbooks continued to consider Xenoturbella as a prim-itive flatworm. New studies were obviously needed to advancethe understanding of its phylogenetic position, and a numberof TEM studies have appeared.The thick epithelium of cells with numerous cilia and largemucus cells were studied by Franze´n and Afzelius (1987),Lundin (1997, 1998), Pedersen and Pedersen (1988), andRohde et al. (1988), all of whom noticed distinct similarities inboth ciliary roots and ciliary tips in Xenoturbella, acoels andnemertodermatids. Also a very unusual process of withdraw-ing and resorbing epithelial cells was observed in all the threegroups (Lundin 2001). A study of the musculature led Ehlersand Sopott-Ehlers (1997) to place Xenoturbella as the sistertaxon of all other bilaterians. The nervous system is a diffuse,intraepithelial net without any special concentrations (Raik-ova et al. 2000). The nervous systems of acoels and nemert-odermatids are rather similar but with an anteriorconcentration (Raikova et al. 2004a,b). All three groupshave an anterior statocyst, which is of rather similar structurein acoels and nemertodermatids, but quite different inXenoturbella (Ehlers 1991). Israelsson (2007) even doubtedits function as a statocyst. The spermatozoa are of a gener-alized metazoan type (Obst et al. in press). There has beenconfusion about the nature of the developmental stages foundinside Xenoturbella, and it seems most safe to state that itsembryology is presently unknown. Only some TEM studies ofthe extracellular matrix (Pedersen and Pedersen 1986) andimmune reactions of the nervous system (Stach et al. 2005)hint to a closer relationship to enteropneusts. A formal clad-istic analysis of morphological characters (Haszprunar 1996)placed Xenoturbella with the acoelomorphs.The morphological evidence seems to be overwhelming infavor of treating Xenoturbellida, Acoela, and Nemertider-matida as one group, the Acoelomorpha. Both morphologicaland numerous molecular phylogenetic analyses have demon-strated beyond doubt that acoels and nemertodermatids arebasal bilaterians, but whether they are sister groups (Hejnolet al. 2009) or separate side branches from the lineage towardthe Eubilateria (e.g., Paps et al. 2009) remains uncertain.However, molecular phylogeny has over the last decadesent Xenoturbella on a long journey across the animal king-dom. It started with a COI analysis (Nore´n and Jondelius1997), which showed Xenoturbella and bivalves as sistergroups, and this found some support from studies of oogen-esis (Israelsson 1997). This interpretation was challenged byBourlat et al. (2003) who analyzed 18S rRNA, and COI and II,and showed that the molluscan RNA was from Xenoturbella’sFig.1. Xenoturbella westbladi living specimen from the Gullmar-fjord, Sweden. Size 1–2mm. Photo courtesy of Dr. Max Telford(University College London).